Advertisement

Ecosystems

, Volume 21, Issue 7, pp 1364–1376 | Cite as

A Framework for Understanding Variation in Pelagic Gross Primary Production of Lake Ecosystems

  • Patrick T. KellyEmail author
  • Christopher T. Solomon
  • Jacob A. Zwart
  • Stuart E. Jones
Article

Abstract

Light and nutrient availability are key physiological constraints for primary production. Widespread environmental changes are causing variability in loads of terrestrial dissolved organic carbon (DOC) and nutrients from watersheds to lakes, contributing to simultaneous changes in both light and nutrient supply. Experimental evidence highlights the potential for these watershed loads to create complex and context-dependent responses of within-lake primary production; however, the field lacks a predictive model to investigate these responses. We embedded a well-established physiological model of phytoplankton growth within an ecosystem model of nutrient and DOC supply to assess how simultaneous changes in DOC and nutrient loads could impact pelagic primary production in lakes. The model generated a unimodal relationship between GPP and DOC concentration when loads of DOC and nutrients were tightly correlated across space or time. In this unimodal relationship, the magnitude of the peak GPP was primarily determined by the DOC-to-nutrient ratio of the load, and the location of the peak along the DOC axis was primarily determined by lake area. Greater nutrient supply relative to DOC load contributed to greater productivity, and larger lake area increased light limitation for primary producers at a given DOC concentration, owing to the positive relationship between lake area and epilimnion depth. When loads of DOC and nutrients were not tightly correlated in space or time, the model generated a wedge-shaped pattern between GPP and DOC, consistent with spatial surveys from a global set of lakes. Our model is thus capable of unifying the diversity of empirically observed spatial and temporal responses of lake productivity to DOC and mineral nutrient supply presented in the literature, and provides qualitative predictions for how lake pelagic primary productivity may respond to widespread environmental changes.

Keywords

gross primary production dissolved organic carbon nutrient loads phytoplankton ecosystem model light limitation 

Notes

Acknowledgements

This project benefited from National Science Foundation support under award DEB-1552343 to SEJ, and an NSERC Discovery grant to CTS. JAZ was supported by the National Science Foundation Graduate Research Fellowship award DGE-1313583. We thank B. Weidel for discussions and ideas contributing to this manuscript. We thank S. Diehl and one anonymous reviewer for their extremely helpful comments for improving the model and the manuscript.

References

  1. Abell JM, Özkundakci D, Hamilton DP, Miller SD. 2011. Relationships between land use and nitrogen and phosphorus in New Zealand lakes. Marine and Freshwater Research 62:162–75.CrossRefGoogle Scholar
  2. Anderson T. 1997. Pelagic nutrient cycles: herbivores as sources and sinks. New York, New York, USA: Springer-Verlag.CrossRefGoogle Scholar
  3. Arbuckle KE, Downing JA. 2001. The influence of watershed land use on lake N : P in a predominantly agricultural landscape. Limnology and Oceanography 46:970–5.CrossRefGoogle Scholar
  4. Ask J, Karlsson J, Persson L, Ask P, Byström P, Jansson M. 2009. Terrestrial organic matter and light penetration: Effects on bacterial and primary production in lakes. Limnology and Oceanography 54:2034–40.CrossRefGoogle Scholar
  5. Berger SA, Diehl S, Kunz TJ, Albrecht D, Oucible AM, Ritzer S. 2006. Light supply, phytoplankton biomass, and seston stoichiometry in a gradient of lake mixing depths. Limnology and Oceanography 51:1898–905.CrossRefGoogle Scholar
  6. Carpenter S, Caraco N, Correll D, Howarth RW, Sharpley AN, Smith VH. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8:559–68.CrossRefGoogle Scholar
  7. Cooke S, Prepas EE. 1998. Stream phosphorus and nitrogen export from agricultural and forested watersheds on the Boreal Plain. Canadian Journal of Fisheries and Aquatic Science 55:2292–9.CrossRefGoogle Scholar
  8. Curtis PJ, Schindler DW. 1997. Hydrologic control of dissolved organic matter in low-order Precambrian Shield Lakes. Biogeochemistry 36:125–38.CrossRefGoogle Scholar
  9. Diehl S, Berger S, Ptacnik R, Wild A. 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: Field experiments. Ecology 83:399–411.CrossRefGoogle Scholar
  10. Diehl S. 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: Theory. Ecology 83:386–98.CrossRefGoogle Scholar
  11. Dillon PJ, Molot LA. 1997. Effect of landscape form on export of dissolved organic carbon, iron, and phosphorus from forested stream catchments. Water Resources Research 33:2591–600.CrossRefGoogle Scholar
  12. Dillon PJ, Rigler FH. 1974. Phosphorus-chlorophyll relationship in lakes. Limnology and Oceanography 19:767–73.CrossRefGoogle Scholar
  13. Edwards KF, Litchman E, Klausmeier CA. 2013. Functional traits explain phytoplankton responses to environmental gradients across lakes of the United States. Ecology 94:1626–35.CrossRefGoogle Scholar
  14. Fee EJ. 1976. The vertical and seasonal distribution of chlorophyll in lakes of the Experimental Lakes Area, northwestern Ontario: Implications for primary production estimates. Limnology and Oceanography 21:767–83.CrossRefGoogle Scholar
  15. Fee EJ, Hecky RE, Kasian SEM, Cruikshank DR. 1996. Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes. Limnology 41:912–20.Google Scholar
  16. Finstad AG, Helland IP, Ugedal O, Hesthagen T, Hessen DO. 2014. Unimodal response of fish yield to dissolved organic carbon. Ecology Letters 17:36–43.CrossRefGoogle Scholar
  17. Fraterrigo JM, Downing JA. 2008. The influence of land use on lake nutrients varies with watershed transport capacity. Ecosystems 11:1021–34.CrossRefGoogle Scholar
  18. Giling DP, Nejstgaard JC, Berger SA, Grossart HP, Kirillin G, Penske A, Lentz M, Casper P, Sareyka J, Gessner MO. 2017. Thermocline deepening boosts ecosystem metabolism: evidence from a large-scale lake enclosure experiment simulating a summer storm. Global Change Biology 23:1448–62.CrossRefGoogle Scholar
  19. Hanson PC, Bade DL, Carpenter SR, Kratz TK. 2003. Lake metabolism: Relationships with dissolved organic carbon and phosphorus. Limnology and Oceanography 48:1112–19.CrossRefGoogle Scholar
  20. Hanson PC, Hamilton DP, Stanley EH, Preston N, Langman OC, Kara EL. 2011. Fate of allochthonous dissolved organic carbon in lakes: A quantitative approach. PLoS One 6.CrossRefGoogle Scholar
  21. Houlahan JE, Mckinney ST, Anderson TM, Mcgill BJ. 2017. The priority of prediction in ecological understanding. Oikos 126:1–7.CrossRefGoogle Scholar
  22. Houser JN. 2006. Water color affects the stratification, surface temperature, heat content, and mean epilimnetic irradiance of small lakes. Canadian Journal of Fisheries and Aquatic Science 63:2447–55.CrossRefGoogle Scholar
  23. Huisman J, Weissing FJ. 1994. Light-limited growth and competition for light in well-mixed aquatic environments: An elementary model. Ecology 75:507–20.CrossRefGoogle Scholar
  24. Imberger J, Parker G. 1985. Mixed layer dynamics in a lake exposed to a spatially-variable wind-field. The priority of prediction in ecological understanding 30:473–88.Google Scholar
  25. Jäger CG, Diehl S. 2014. Resource competition across habitat boundaries: Asymmetric interactions between benthic and pelagic producers. Ecological Monographs 84:287–302.CrossRefGoogle Scholar
  26. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M. 2009. Light limitation of nutrient-poor lake ecosystems. Nature 460:506–9.CrossRefGoogle Scholar
  27. Kirk JT. 1994. Light and photosynthesis in aquatic ecosystems. 2nd ed.Google Scholar
  28. Kratz TK, Deegan LA, Harmon ME, Lauenroth WK. 2003. Ecological Variability in Space and Time: Insights Gained from the US LTER Program. Bioscience 53:57.CrossRefGoogle Scholar
  29. Kunz TJ, Diehl S. 2003. Phytoplankton, light and nutrients along a gradient of mixing depth: A field test of producer-resource theory. Freshwater Biology 48:1050–63.CrossRefGoogle Scholar
  30. Lennon JT, Pfaff LE. 2005. Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquatic Microbial Ecology 39:107–19.CrossRefGoogle Scholar
  31. Mazumder A, Taylor WD. 1994. Thermal structure of lakes varying in size and water clarity. Limnology and Oceanography 39:968–76.CrossRefGoogle Scholar
  32. Molot LA, Dillon PJ. 1997. Colour - mass balances and colour – dissolved organic carbon relationships in lakes and streams in central Ontario. Canadian Journal of Fisheries and Aquatic Sciences 54:2789–95.CrossRefGoogle Scholar
  33. Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Høgåsen T, Wilander A, Skjelkvåle BL, Jeffries DS, Vuorenmaa J, Keller B, Kopácek J, Vesely J. 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:537–40.CrossRefGoogle Scholar
  34. Morris DP, Zagarese H, Williamson CE, Balseiro EG, Hargreaves BR, Modenutti B, Moeller R, Queimalinos C. 1995. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40:1381–91.CrossRefGoogle Scholar
  35. Obrador B, Staehr P, Christensen JPC. 2014. Vertical patterns of metabolism in three contrasting stratified lakes. Limnology and Oceanography 59:1228–40.CrossRefGoogle Scholar
  36. Pérez-Fuentetaja A, Dillon PJ, Yan ND, McQueen DJ. 1999. Significance of dissolved organic carbon in the prediction od thermocline depth in small Canadian shield lakes. Ecosystems 33:127–33.Google Scholar
  37. Raike A, Pietilainen OP, Rekolainen S, Kauppila P, Pitkanen H, Niemi J, Raateland A, Vuorenmaa J. 2003. Trends of phosphorus, nitrogen and chlorophyll a concentrations in Finnish rivers and lakes in 1975-2000. Sci Total Environ 310:47–59.CrossRefGoogle Scholar
  38. Rastetter EB, Aber JD, Peters DPC, Ojima DS, Burke IC. 2003. Using mechanistic models to scale ecological processes across space and time. Bioscience 53:68.CrossRefGoogle Scholar
  39. Read JS, Hamilton DP, Desai AR, Rose KC, MacIntyre S, Lenters JD, Smyth RL, Hanson PC, Cole JJ, Staehr PA, Rusak JA, Pierson DC, Brookes JD, Laas A, Wu CH. 2012. Lake-size dependency of wind shear and convection as controls on gas exchange. Geophysical Research LettersGoogle Scholar
  40. Read JS, Rose KC. 2013. Water color affects the stratification, surface temperature, heat content, and mean epilimnetic irradiance of small lakes. Limnology and Oceanography 58:921–31.CrossRefGoogle Scholar
  41. Sato H, Itoh A, Kohyama T. 2007. SEIB-DGVM: A new dynamic global vegetation model using a spatially explicit individual-based approach. Ecological Modelling 200:279–307.CrossRefGoogle Scholar
  42. Schindler DW. 1977. Evolution of phosphorus limitation in lakes. Science 195:260–2.CrossRefGoogle Scholar
  43. Seekell DA, Lapierre J, Karlsson J. 2015. Trade-offs between light and nutrient availability across gradients of dissolved organic carbon concentration in Swedish lakes : implications for patterns in primary production. Can J Fish Aquatic Science 9:1–9.Google Scholar
  44. Solomon CT, Brusewitz DA, Richardson DC, Rose KC, Van de Bogert MC, Hanson PC, Kratz TK, Larget B, Adrian R, Babin BL, Chiu CY, Hamilton DP, Gaiser EE, Hendrick S, Istvanovics V, Laas A, O’Donnell DM, Pace ML, Ryder E, Staehr PA, Torgersen T, Vanni MJ, Weathers KC, Zhu GW. 2013. Ecosystem respiration: Drivers of daily variability and background respiration in lakes around the globe. Limnology and Oceanography 58:849–66.CrossRefGoogle Scholar
  45. Sterner RW. 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93:433–45.CrossRefGoogle Scholar
  46. Thrane JE, Hessen DO, Anderson T. 2014. The absorption of light in lakes: Negative impact of dissolved organic carbon on primary productivity. Ecosystems 17:1040–52.CrossRefGoogle Scholar
  47. Tranvik LJ, Downing JA, Cotner J, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K et al. 2009. Lakes and reservoirs as regulators of carbon cycling and climate. Limnology and Oceanography 54:2298–314.CrossRefGoogle Scholar
  48. Vitousek PM, Reiners WA. 1975. Ecosystem succession and nutrient retention - hypothesis. Bioscience 25:376–81.CrossRefGoogle Scholar
  49. von Einem J, Granéli W. 2010. Effects of fetch and dissolved organic carbon on epilimnion depth and light climate in small forest lakes in southern Sweden. Limnology and Oceanography 55:920–30.CrossRefGoogle Scholar
  50. Williamson CE, Stemberger RS, Morris DP, Frost TM, Paulsen SG. 1996. Ultraviolet radiation in North American lakes: attenuation estimates from DOC measurements and implications for plankton communities. Limnology and Oceanography 41:1024–34.CrossRefGoogle Scholar
  51. Zwart JA, Craig N, Kelly PT, Sebestyen SD, Solomon CT, Weidel BC, Jones SE. 2016. Metabolic and physiochemical responses to a whole-lake experimental increase in dissolved organic carbon in a north-temperate lake. Limnology and Oceanography 61:723–34.CrossRefGoogle Scholar
  52. Zwart JA, Solomon CT, Jones SE. 2015. Phytoplankton traits predict ecosystem function in a global set of lakes. Ecology 96:2257–64.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Patrick T. Kelly
    • 1
    Email author
  • Christopher T. Solomon
    • 2
  • Jacob A. Zwart
    • 3
  • Stuart E. Jones
    • 3
  1. 1.Department of BiologyMiami UniversityOxfordUSA
  2. 2.Cary Institute of Ecosystem StudiesMillbrookUSA
  3. 3.Department of Biological SciencesUniversity of Notre DameNotre DameUSA

Personalised recommendations